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      Early detection of consciousness in patients with acute severe traumatic brain injury

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          Abstract

          See Schiff (doi: [Related article:]10.1093/awx209) for a scientific commentary on this article.

          Bedside examination does not reliably detect consciousness in patients with acute severe traumatic brain injury. Edlow, Chatelle et al. report that stimulus-based functional MRI and EEG techniques enhance early detection of consciousness and cortical responses to language in these patients, which could alter time-sensitive decisions about withdrawal of life-sustaining therapies.

          Abstract

          See Schiff (doi: [Related article:]10.1093/awx209) for a scientific commentary on this article.

          Patients with acute severe traumatic brain injury may recover consciousness before self-expression. Without behavioural evidence of consciousness at the bedside, clinicians may render an inaccurate prognosis, increasing the likelihood of withholding life-sustaining therapies or denying rehabilitative services. Task-based functional magnetic resonance imaging and electroencephalography techniques have revealed covert consciousness in the chronic setting, but these techniques have not been tested in the intensive care unit. We prospectively enrolled 16 patients admitted to the intensive care unit for acute severe traumatic brain injury to test two hypotheses: (i) in patients who lack behavioural evidence of language expression and comprehension, functional magnetic resonance imaging and electroencephalography detect command-following during a motor imagery task (i.e. cognitive motor dissociation) and association cortex responses during language and music stimuli (i.e. higher-order cortex motor dissociation); and (ii) early responses to these paradigms are associated with better 6-month outcomes on the Glasgow Outcome Scale-Extended. Patients underwent functional magnetic resonance imaging on post-injury Day 9.2 ± 5.0 and electroencephalography on Day 9.8 ± 4.6. At the time of imaging, behavioural evaluation with the Coma Recovery Scale-Revised indicated coma ( n = 2), vegetative state ( n = 3), minimally conscious state without language ( n = 3), minimally conscious state with language ( n = 4) or post-traumatic confusional state ( n = 4). Cognitive motor dissociation was identified in four patients, including three whose behavioural diagnosis suggested a vegetative state. Higher-order cortex motor dissociation was identified in two additional patients. Complete absence of responses to language, music and motor imagery was only observed in coma patients. In patients with behavioural evidence of language function, responses to language and music were more frequently observed than responses to motor imagery (62.5–80% versus 33.3–42.9%). Similarly, in 16 matched healthy subjects, responses to language and music were more frequently observed than responses to motor imagery (87.5–100% versus 68.8–75.0%). Except for one patient who died in the intensive care unit, all patients with cognitive motor dissociation and higher-order cortex motor dissociation recovered beyond a confusional state by 6 months. However, 6-month outcomes were not associated with early functional magnetic resonance imaging and electroencephalography responses for the entire cohort. These observations suggest that functional magnetic resonance imaging and electroencephalography can detect command-following and higher-order cortical function in patients with acute severe traumatic brain injury. Early detection of covert consciousness and cortical responses in the intensive care unit could alter time-sensitive decisions about withholding life-sustaining therapies.

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          Conscious, preconscious, and subliminal processing: a testable taxonomy.

          Of the many brain events evoked by a visual stimulus, which are specifically associated with conscious perception, and which merely reflect non-conscious processing? Several recent neuroimaging studies have contrasted conscious and non-conscious visual processing, but their results appear inconsistent. Some support a correlation of conscious perception with early occipital events, others with late parieto-frontal activity. Here we attempt to make sense of these dissenting results. On the basis of the global neuronal workspace hypothesis, we propose a taxonomy that distinguishes between vigilance and access to conscious report, as well as between subliminal, preconscious and conscious processing. We suggest that these distinctions map onto different neural mechanisms, and that conscious perception is systematically associated with surges of parieto-frontal activity causing top-down amplification.
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            Willful modulation of brain activity in disorders of consciousness.

            The differential diagnosis of disorders of consciousness is challenging. The rate of misdiagnosis is approximately 40%, and new methods are required to complement bedside testing, particularly if the patient's capacity to show behavioral signs of awareness is diminished. At two major referral centers in Cambridge, United Kingdom, and Liege, Belgium, we performed a study involving 54 patients with disorders of consciousness. We used functional magnetic resonance imaging (MRI) to assess each patient's ability to generate willful, neuroanatomically specific, blood-oxygenation-level-dependent responses during two established mental-imagery tasks. A technique was then developed to determine whether such tasks could be used to communicate yes-or-no answers to simple questions. Of the 54 patients enrolled in the study, 5 were able to willfully modulate their brain activity. In three of these patients, additional bedside testing revealed some sign of awareness, but in the other two patients, no voluntary behavior could be detected by means of clinical assessment. One patient was able to use our technique to answer yes or no to questions during functional MRI; however, it remained impossible to establish any form of communication at the bedside. These results show that a small proportion of patients in a vegetative or minimally conscious state have brain activation reflecting some awareness and cognition. Careful clinical examination will result in reclassification of the state of consciousness in some of these patients. This technique may be useful in establishing basic communication with patients who appear to be unresponsive. 2010 Massachusetts Medical Society
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              Diagnostic accuracy of the vegetative and minimally conscious state: Clinical consensus versus standardized neurobehavioral assessment

              Background Previously published studies have reported that up to 43% of patients with disorders of consciousness are erroneously assigned a diagnosis of vegetative state (VS). However, no recent studies have investigated the accuracy of this grave clinical diagnosis. In this study, we compared consensus-based diagnoses of VS and MCS to those based on a well-established standardized neurobehavioral rating scale, the JFK Coma Recovery Scale-Revised (CRS-R). Methods We prospectively followed 103 patients (55 ± 19 years) with mixed etiologies and compared the clinical consensus diagnosis provided by the physician on the basis of the medical staff's daily observations to diagnoses derived from CRS-R assessments performed by research staff. All patients were assigned a diagnosis of 'VS', 'MCS' or 'uncertain diagnosis.' Results Of the 44 patients diagnosed with VS based on the clinical consensus of the medical team, 18 (41%) were found to be in MCS following standardized assessment with the CRS-R. In the 41 patients with a consensus diagnosis of MCS, 4 (10%) had emerged from MCS, according to the CRS-R. We also found that the majority of patients assigned an uncertain diagnosis by clinical consensus (89%) were in MCS based on CRS-R findings. Conclusion Despite the importance of diagnostic accuracy, the rate of misdiagnosis of VS has not substantially changed in the past 15 years. Standardized neurobehavioral assessment is a more sensitive means of establishing differential diagnosis in patients with disorders of consciousness when compared to diagnoses determined by clinical consensus.
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                Author and article information

                Contributors
                Journal
                Brain
                Brain
                brainj
                Brain
                Oxford University Press
                0006-8950
                1460-2156
                September 2017
                20 July 2017
                01 September 2018
                : 140
                : 9
                : 2399-2414
                Affiliations
                [1 ]Center for Neurotechnology and Neurorecovery, Massachusetts General Hospital, 175 Cambridge Street, Boston, MA, 02114, USA
                [2 ]Department of Neurology, Massachusetts General Hospital, Harvard Medical School, 175 Cambridge Street, Boston, MA, 02114, USA
                [3 ]Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, 149 13th Street, Charlestown, MA 02129, USA
                [4 ]Coma Science Group, GIGA Consciousness, University and University Hospital of Liège, Liège, Belgium
                [5 ]Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital, Harvard Medical School, 300 First Avenue, Charlestown, MA, 02129, USA
                [6 ]Department of Physical Medicine and Rehabilitation, Massachusetts General Hospital, Harvard Medical School, 55 Fruit Street, Boston, MA, 02114, USA
                [7 ]Department of Engineering, Brown University, 184 Hope St, Providence, RI, 02912, USA
                Author notes
                Correspondence to: Brian L. Edlow, MD Center for Neurotechnology and Neurorecovery Massachusetts General Hospital 175 Cambridge Street – Suite 300 Boston, MA 02114, USA E-mail: bedlow@ 123456mgh.harvard.edu Web: www.massgeneral.org/nicc

                Brian L. Edlow, Camille Chatelle, Eric S. Rosenthal and Ona Wu authors contributed equally to this work.

                See Schiff (doi: [Related article:]10.1093/awx209) for a scientific commentary on this article.

                Article
                PMC6059097 PMC6059097 6059097 awx176
                10.1093/brain/awx176
                6059097
                29050383
                f21e4138-6c19-4694-a60a-146edbbc9e87
                © The Author (2017). Published by Oxford University Press on behalf of the Guarantors of Brain. All rights reserved. For Permissions, please email: journals.permissions@oup.com
                History
                : 14 February 2017
                : 19 May 2017
                : 29 May 2017
                Page count
                Pages: 16
                Funding
                Funded by: National Institutes of Health 10.13039/100000002
                Award ID: K23NS094538
                Funded by: American Academy of Neurology 10.13039/100005339
                Funded by: American Brain Foundation 10.13039/100005331
                Categories
                Original Articles

                traumatic brain injury,consciousness,functional MRI,EEG,intensive care unit

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